Research Article Antioxidant Potential of Spirulina platensis...

Research ArticleAntioxidant Potential of Spirulina platensisMitigates Oxidative Stress and Reprotoxicity Inducedby Sodium Arsenite in Male Rats

Samir A. E. Bashandy,1 Sally A. El Awdan,1 Hossam Ebaid,2,3 and Ibrahim M. Alhazza2

1Pharmacology Department, National Research Center, El Buhouth Street, Dokki, Giza 12311, Egypt2Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia3Zoology Department, College of Science, Minia University, Minia 11432, Egypt

Correspondence should be addressed to Samir A. E. Bashandy; [email protected]

Received 22 October 2015; Revised 7 December 2015; Accepted 15 December 2015

Academic Editor: Ilaria Peluso

Copyright © 2016 Samir A. E. Bashandy et al. This is an open access article distributed under the Creative Commons AttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properlycited.

The present study aimed to examine the protective role of Spirulina platensis (S. platensis) against arsenic-induced testicularoxidative damage in rats. Arsenic (in the form of NaAsO

2at a dose of 6.3mg/kg body weight for 8 weeks) caused a significant

accumulation of arsenic in testicular tissues as well as a decrease in the levels of testicular superoxide dismutase (SOD), catalase(CAT), reduced glutathione, and zinc. Moreover, it significantly decreased plasma testosterone, luteinizing hormone (LH),triiodothyronine (T

3), and thyroxine (T

4) levels and reduced sperm motility and sperm count. Arsenic (AS) led to a significant

increase in testicularmalondialdehyde (MDA), tumour necrosis factor alpha (TNF-𝛼), nitric oxide (NO), and sperm abnormalities.S. platensis at a dose of 300mg/kg was found to attenuate As-induced oxidative stress, testicular damage, and sperm abnormalitiesby its potent antioxidant activity. S. platensismay represent a potential therapeutic option to protect the testicular tissue from arsenicintoxication.

1. Introduction

Arsenic contamination occurs due to its industrial uses inthe production of agricultural pesticides, wood preservatives,and glass production and inmedicine [1, 2]. Arsenic exposurecauses obvious damage in various organs, including the malereproductive function as manifested by decrease of andro-genesis, suppression of spermatogenesis, and a reduction inthe weight of testes and sex organs [3, 4]. However, emergingevidence supports the role of oxidative stress and inflamma-tionwith increased production of proinflammatory cytokinesin the pathogenesis of arsenic-induced organ damage [5, 6].Also, previous studies revealed that several antioxidant agentssignificantly protected against tissue damage due to arsenicintoxication [6, 7].

The cyanobacterium Spirulina is a filamentous blue-greenalga belonging to the Oscillatoriaceae family that is generallyfound in tropical and subtropical regions in warm alkaline

water. Spirulina is characterized by high nutritional valuewhere it contains high protein content (60–70% by dryweight), plenty of vitamins, amino acids, gamma-linoleicacid, and minerals [8]. The consumption of Spirulina asa diet supplement has health benefits in preventing ormanaging hypercholesterolemia [9], hyperglycerolemia [10],obesity, inflammation [11], cancer [12], and cardiovasculardisease [13]. In addition, Spirulina has antidiabetic effect[14]. Spirulina provides protection against mercuric chloride-induced oxidative stress and alteration of antioxidant defensemechanism in the liver.These activities were largely related tophycocyanin, an active protein of Spirulina [15]. Phycocyanin(Pc) is a biliprotein of the blue-green alga. This proteincontains a tetrapyrrole phycocyanobilin, which is responsiblefor antioxidant properties of Pc [16]. It has been reportedthat Pc has significant antioxidant and radical scavengingproperties, offering protection against oxidative stress [17].Antioxidants can reduce arsenic toxicity through chelating

Hindawi Publishing CorporationOxidative Medicine and Cellular LongevityVolume 2016, Article ID 7174351, 8 pageshttp://dx.doi.org/10.1155/2016/7174351

2 Oxidative Medicine and Cellular Longevity

it and scavenging free radicals [18]. It was reported that Pccan bind with heavy metals [19]; hence, it can chelate andremove them. In viewof the above concerns, the present studywas designed to evaluate the antioxidant action of S. platensisenrichedwith phenolic compounds in ameliorating testiculardysfunction and oxidative stress induced by arsenic.

2. Materials and Methods

2.1. Test Chemicals. Sodium arsenite was purchased fromMerck, Germany, while S. platensis was obtained fromAlibaba Comp., China, in the form of powder.

2.2. Animals. Four-month male Wistar albino rats, weight-ing 180–200 g, were got from the animal house, Facultyof Pharmacy, King Saud University. Animals were housedand fed as previously described [20]. The rats were fed acommercially available rat pellet diet ad libitum throughoutthe experimental period. The rats allowed to adapt to labo-ratory environment for seven days before the beginning ofthe experiment. This study was performed in the ZoologyDepartment, Faculty of Science, King Saud University, SaudiArabia. The care and handling of experimental animals werecarried out according to the animal ethical committee of KingSaud University, College of Pharmacy.

2.3. Experimental Protocol. The animals were randomlydivided into four groups, consisting of eight rats in each, andthey were treated for eight weeks as below:

Group I: normal control (rats received only water asvehicle).Group II: rats received orally arsenic as sodiumarsenite, 6.3mg/kg corresponding to 15% of LD50(41mg/Kg) [21].Group III: rats received orally 300mg/Kg of S. platen-sis [22] followed by oral administration of arsenic assodium arsenite 6.3mg/Kg daily.Group IV: rats received orally S. platensis only as ingroup III.

All treatments are carried out daily for eight weeks in orderto evaluate their effects [23]. The rats were subjected toether anesthesia using sliding top chamber (Kent Scientificcorporation) during sample collection.

2.4. Sample Preparation and Biochemical Analysis. At theend of the experimentation period, blood and organswere collected as previously described [20]. Plasma testos-terone, luteinizing hormone (LH), triiodothyronine (T

3),

and thyroxine (T4) concentrations were assayed by enzyme

immunoassay using commercial kits from Diagnostic prod-ucts Co., Los Angeles, CA, USA. Testes, vas deferens, epi-didymis, prostate gland, and seminal vesicle were isolatedfrom surrounding tissues and placed into tubes. The organswere dried between two sheets of filter paper and theirwet weight was determined. The organ weight/body weightratio × 100 was calculated and expressed as relative organ

As c

once

ntra

tion

(𝜇g/

g tis

sue)

∗∗

∗∗@

0.0

0.5

1.0

1.5

2.0

SpirulinaArsenic Spirulina + arsenicControl

Figure 1: Effect of Spirulina platensis on testicular arsenic concen-tration (𝜇g/g tissue) in arsenic intoxicated rats. All numbers aremean + standard error, 𝑛 = 8. AS: arsenic. ∗∗Significantly differentfrom control value, ∗∗𝑃 < 0.01. @Significantly different from arsenicgroup value, @𝑃 < 0.01.

weight beside absolute weight. Epididymis and testes wereprocessed as previously described in order to perform histo-logical, biochemical, and sperm analysis [20].

The supernatant of testicular homogenates was usedfor determination of malondialdehyde, reduced glutathione,catalase, and superoxide dismutase levels using colorimet-ric assay kits according to the recommendations of themanufacturer (BioDiagnostic, Egypt). The testicular levelof nitric oxide was assayed using colorimetric assay kitfollowing themanufacturer’s instructions (CaymanChemicalCompany, USA). Also, the level of tumour necrosis factor-𝛼in testicular homogenates was determined by enzyme-linkedimmunosorbent assay (ELISA) using rat TNF-𝛼 immunoas-say kit according to the guidance of the manufacturer (R&DSystems, USA). In addition, arsenic and zinc levels in testeswere estimated by atomic absorption (Perkin-Elmer, UK).

2.5. Sperm Analysis. Sperm motility, count, and abnormali-ties were evaluated as previously described [20, 24].

2.6. Statistical Analysis. All values were expressed as mean ±SE. Statistical analysis of data was performed using two-wayANOVA followed by least significant difference (LSD) forcomparison of various treatments using the spss 13.0.

3. Results

3.1. Biochemical Analysis. The results demonstrated that sup-plementation of Spirulina to arsenic exposed rats reduced thearsenic content remarkably in the testis (Figure 1). On theother hand, testicular zinc concentration of arsenic treatedgroups (Figure 2) decreased significantly as compared withcontrol. Testicular zinc concentration in S. platensis + arsenicgroup is significantly higher than those treated with arseniconly. Arsenic treatment without S. platensis significantlyenhanced the levels of testicular MDA, TNF-𝛼, and nitricoxide concentrations (𝑃 ≤ 0.1), while SOD, catalase, and

Oxidative Medicine and Cellular Longevity 3

Table 1: Effect of S. platensis on testicular oxidative stress parameters in arsenic treated rats.

Parameter TreatmentControl Arsenic S. platensis + arsenic S. platensis

MDA (nmol/mg protein) 10.48 ± 0.36 22.83 ± 0.89∗∗ 14.95 ± 0.65∗∗@ 8.76 ± 0.67∗

SOD (unit/mg protein) 24.27 ± 0.65 9.11 ± 0.35∗∗ 16.81 ± 0.44∗∗@ 26.89 ± 0.21∗∗

Catalase (𝜇mol/min/mg protein) 30.28 ± 1.06 15.86 ± 0.35∗∗ 22.75 ± 0.74∗∗@ 32.11 ± 2.10GSH (nmol/mg protein) 27.25 ± 1.47 14.13 ± 0.89∗∗ 21.25 ± 1.14∗∗@ 39.87 ± 1.86∗∗

TNF-𝛼 (pg/100mg tissue) 11.48 ± 0.21 108.12 ± 3.15∗∗ 46.92 ± 2.71∗∗@ 10.65 ± 0.47Nitric oxide (nmol/100mg tissue) 85.20 ± 4.14 216.92 ± 5.78∗∗ 130.41 ± 6.37∗∗@ 87.14 ± 3.60All numbers are mean + standard error, 𝑛 = 8.∗Significantly different from control value, ∗𝑃 < 0.05, ∗∗𝑃 < 0.01.@Significantly different from arsenic group value, @𝑃 < 0.01.MDA: malondialdehyde; SOD: superoxide dismutase; GSH: reduced glutathione; TNF-𝛼: tumor necrosis factor-alpha.

∗∗

∗∗@

0

5

10

15

20

25

Zinc

conc

entr

atio

n (𝜇

g/g

tissu

e)

SpirulinaArsenicControl Spirulina + arsenic

Figure 2: Effect of Spirulina platensis on testicular zinc concen-tration (𝜇g/g tissue) in arsenic intoxicated rats. All numbers aremean + standard error, 𝑛 = 8. ∗∗Significantly different from controlvalue, ∗∗𝑃 < 0.01. @Significantly different from arsenic group value,@𝑃 < 0.01.

GSH levels decreased significantly as compared with control(Table 1). The administration of S. platensis followed byarsenic intoxication attenuated these effects.

3.2. Reproductive Organ Weights. Sodium arsenite intoxi-cation significantly decreased the testis, vas deferens, epi-didymis, prostate, and seminal vesicle weights. Treatmentwith Spirulina prior to arsenic administration, however, kepttheweight of reproductive organs close to normal (Tables 2(a)and 2(b)).

3.3. Plasma Hormones Level. We observed that sodiumarsenite intoxication decreased the levels of testosterone, LH,T3, andT

4significantly (𝑃 ≤ 0.01) compared to control values

(Figures 3 and 4). Treatment with S. platensiswas found to beeffective in alleviation of alteration in hormone levels inducedby the arsenic.

3.4. SpermMotility, Count, andAbnormalities. Arsenic intox-ication decreased the sperm motility and count comparedto the normal control (Table 3). In addition, a significant

increase of sperm abnormalities was found in rats treatedwith arsenic. S. platensis administration reduced the toxiceffects of arsenic on sperms.

3.5. Histopathological Observation. Histological observationof the testes of control animals showednormal spermatogeniccells with normal arrangement (Figure 5(a)). The section oftestis of arsenic treated rat showed (Figure 5(b)) thickening oftubules basement membrane, vascular degeneration, markeddecrease in spermatogenic cells population, hemorrhage ininterstitial tissues, and deformation of Leydig cells.Moreover,the sperm bundles were absent in some tubules. Pretreatmentwith S. platensis could, however, prevent the As-toxicityand maintain the normalcy of the testicular architecture(Figure 5(c)).

4. Discussion

The response of male rats to the protective effects of S.platensis against arsenic-induced oxidative stress and repro-toxicity was examined in this study. Our results proposedthat the increase of testicular MDA level may result fromarsenic accumulation in the testis suggesting oxidative stressfollowing free radical generation. Enhancement of lipidperoxidation and inhibition of the antioxidant enzymes inthe testes are importantmechanisms for arsenic pathogenesis[25]. The testicular tissue is provided with an antioxidantdefense system including several enzymes functioning in acollective manner for the removing free radicals generatedwithin the cell. SOD and catalase are major enzymes that getrid of reactive oxygen species (ROS) [26]. In the present study,the animals treated with arsenic showed decreased activitiesof testicular antioxidant enzymes, SOD, and CAT that mayindicate the antioxidant imbalance induced by arsenic. Adecrease in the activity of SOD can be referred to as anenhanced superoxide production during arsenicmetabolism.SOD catalyzes the dismutation of superoxide anions andprevents the subsequent formation of hydroxyl radicals [27].The observed decreased testicular SOD might be responsiblefor increased lipid peroxidation following arsenic treatment[28]. The superoxide radical also reduced the activity ofcatalase [29]. Moreover, exposure to arsenic reduces the


Table 2: (a) Absolute reproductive organ weights (g) of arsenic intoxicated rats treated with S. platensis. (b) Effect of S. platensis onreproductive organ weights (g) relative to body weight in arsenic intoxified rats.

(a)


Left testis 1.76 ± 0.05 1.40 ± 0.07∗∗ 1.67 ± 0.05@ 1.79 ± 0.08Vas deferens 0.21 ± 0.01 0.13 ± 0.01∗∗ 0.17 ± 0.007∗∗ 0.19 ± 0.006Epididymis 0.86 ± 0.03 0.57 ± 0.02∗∗ 0.73 ± 0.03∗ 0.81 ± 0.04Prostate 0.80 ± 0.02 0.37 ± 0.03∗∗ 0.65 ± 0.05∗∗@ 0.77 ± 0.05Seminal vesicle 1.51 ± 0.08 0.86 ± 0.06∗∗ 1.18 ± 0.06∗∗@ 1.46 ± 0.07

(b)

TreatmentParameter Control Arsenic S. platensis + arsenic S. platensisLeft testis 0.62 ± 0.02 0.51 ± 0.02∗∗ 0.59 ± 0.01@ 0.60 ± 0.02Vas deferens 0.07 ± 0.003 0.05 ± 0.002∗∗ 0.05 ± 0.002∗∗ 0.06 ± 0.005Epididymis 0.25 ± 0.002 0.21 ± 0.006∗∗ 0.23 ± 0.007∗ 0.24 ± 0.008Prostate 0.31 ± 0.02 0.13 ± 0.01∗∗ 0.20 ± 0.009∗∗@ 0.29 ± 0.01Seminal vesicle 0.52 ± 0.01 0.31 ± 0.01∗∗ 0.47 ± 0.02∗@ 0.50 ± 0.04All numbers are mean + standard error, 𝑛 = 8.∗Significantly different from control value, ∗𝑃 < 0.05, ∗∗𝑃 < 0.01.@Significantly different from arsenic group value, @𝑃 < 0.01.

Table 3: Effect of S. platensis on sperm morphological parameters in experimental arsenic exposed rats.


Sperm motility (%) 83.56 ± 1.18 72.29 ± 2.00∗∗ 84.56 ± 0.67@ 90.42 ± 2.10∗

Sperm count per epididymis(million/epididymis) 17.47 ± 1.06 7.09 ± 0.41∗∗ 12.68 ± 0.85∗∗@ 25.5 ± 1.15∗∗

Abnormal sperm rate (%)Head 2.16 ± 0.13 8.92 ± 0.56∗∗ 4.94 ± 0.19∗∗@ 1.90 ± 0.07Tail 1.83 ± 0.11 2.88 ± 0.14∗∗ 2.14 ± 0.18@ 2.11 ± 0.12Total 3.99 ± 0.14 11.34 ± 0.51∗∗ 6.92 ± 0.32∗∗@ 4.00 ± 0.16

All numbers are mean + standard error, 𝑛 = 8.∗Significantly different from control value, ∗𝑃 < 0.05, ∗∗𝑃 < 0.01.@Significantly different from arsenic group value, @𝑃 < 0.01.

testicular GSH content of the present rats as previously found[30, 31].

The improved antioxidant status of testicular tissues byS. platensis can be deduced from elevated levels of testicularSOD, CAT, zinc, and GSH and a decrease of MDA andarsenic concentrations of S. platensis + arsenic group ascompared to arsenic group. The antioxidant properties ofS. platensis may be attributed to the presence of potentantioxidant components as 𝛽-carotene, vitamin C, vitaminE, selenium, andmanganese [32–37].Moreover, phycocyaninof S. platensis significantly inhibited peroxyl radical inducedlipid peroxidation [16] and it may chelate arsenic as it bindswith heavy metals [38].

Free radicals are able to induce cytokine production fromvarious cell types [39]. The decreased antioxidant enzyme

activities with elevated lipid peroxidation, TNF-𝛼, and NOlevels indicated impaired antioxidative defense mechanismswith an oxidative injury in the testes of arsenic group. Itwas reported that there was a link between TNF-𝛼 or NOand oxidative stress. Both TNF-𝛼 and NO can increase theproduction of reactive oxygen species and oxidative stress[40, 41]. It was found that both NO and TNF-𝛼 inhibitedtestosterone synthesis pathways [42, 43]. The significantdecrease in the plasma level of testosterone in the presentrats treated with arsenic may be due to its direct effect onthe testis or suppression of luteinizing hormone secretion. S.platensis represses proinflammatory cytokine expression andsecretion through suppression of nuclear factor kappa (NF-𝜅B). Activation of NF-𝜅B pathway is a major pathway for thedevelopment of inflammatory diseases [44].The antioxidants


∗∗

∗∗

∗∗@

∗∗@

0

1

2

3

4Te

stoste

rone

leve

l (ng

/mL)

ArsenicControl SpirulinaSpirulina + arsenic

ArsenicControl SpirulinaSpirulina + arsenic0.0

0.5

1.0

1.5

LH le

vel (

ng/m

L)

Figure 3: Effect of S. platensis onplasma testosterone and luteinizinghormone (LH) levels in arsenic intoxicated rats. All numbers aremean + standard error, 𝑛 = 8. ∗∗Significantly different from controlvalue, ∗∗𝑃 < 0.01. @Significantly different from arsenic group value,@𝑃 < 0.01.

found in S. platensis maintain the endogenous antioxidantsand inhibit elevation of testicularNO andTNF-𝛼, thus reduc-ing oxidative stress and relieving the pathological changesinduced by arsenic in testis which may lead to improvementof testosterone level.

A significant decrease in the weights of testis andaccessory sex organs was observed in arsenic exposed rats,which may be due to the inhibition of spermatogenesis anddecreased steroidogenesis. It is well known that the testos-terone stimulates normal growth and function of male repro-ductive system [45]. The weight of the testis is also largelydependent on the mass of the differentiated spermatogeniccells and reduction in the testicular weight indicates germcell loss [3]. Our results showed that S. platensis alleviatedthe reduction in T

3and T

4levels induced by arsenic. It is

well known that thyroid hormones affect spermatogenesis[46]. In addition, the number of sperm production by testeswas decreased significantly in hypothyroid rats and increasedin hyperthyroid rats in comparison with the control grouprats. It was shown that thyroid hormone receptor expresses inthe germ cells from spermatogonia to primary spermatocytes[47].

A higher ROS production or a decreased antioxidantcapacity is responsible for stimulation of lipid peroxidationproduction which affects sperm motility [48]. The observeddecrease in the number of sperm count and motility andincrease of sperm morphological abnormalities may result

∗∗

∗∗

∗@

∗∗@

0

1

2

3

4

T3(n

g/m

L)

SpirulinaArsenicControl Spirulina + arsenic

SpirulinaArsenicControl Spirulina + arsenic0

20

40

60

T4(n

mol

/L)

Figure 4: Effect of S. platensis on T3 and T4 concentrations inarsenic intoxicated rats. All numbers are mean + standard error, 𝑛 =8. ∗Significantly different from control value, ∗𝑃 < 0.05, ∗∗𝑃 < 0.01.@Significantly different from arsenic group value, @𝑃 < 0.01. T3:triiodothyronine; T4: thyroxine.

from less production of androgen in arsenic exposed rats orfrom increased level of testicular lipid peroxidation. Sperma-tozoa are particularly liable to ROS-induced damage becausetheir plasmamembranes have large quantities of polyunsatu-rated fatty acids and their cytoplasm comprises low concen-tration of the scavenging enzymes [49]. It is documented thatROS generation can induce abnormal sperm morphology[50]. It appeared that S. platensis, containing potent antiox-idants, significantly reversed the deleterious effects of arsenicon sperms. Thus, the antioxidative properties of S. platensismay play a positive role in the defense against oxidative stressinduced by arsenic. Our previous findings clearly highlightthe role of S. platensis as a protective modulator of mercuricchloride-induced testicular injuries and oxidative stress [20].Here, S. platensis significantly lessen the increase in arsenicconcentration, and the reduction in zinc concentration of tes-ticular tissue resulted from sodium arsenite administration.Zinc acts as a cofactor for superoxide dismutase, preservesthe reduced glutathione, and induces metallothionein whichhas antioxidant andmetal-chelating properties [51]. Zinc actsas an effective anti-inflammatory and antioxidant agent [52].It can be speculated that S. platensis through its antioxidantactivity decreased the arsenic burden in testicular tissue andrestored the depleted zinc which results in an additionalprotective effect against arsenic-mediated testicular toxicity.

The present investigation showed that the treatment ofthe rats with S. platensis improves sperm characteristics as


(a) (b)

(c) (d)

Figure 5: (a) Photomicrograph of the testis of control rat showing normal structure of seminiferous tubules containing different types ofspermatogenic cells (H&E, ×400). (b) Photomicrograph of the testis of rat that received arsenic showing deformed Leydig cells (white arrow),vacuolated spermatogenic cells (VD), thickened basement membrane (dotted arrow), and congestion of blood vessel (black arrow) (H&E,×400). (c) Photomicrograph of the testis of rat treated with S. platensis + As showing normal spermatogenesis and cell arrangement (H&E,×400). (d) Photomicrograph of the testis of rat treated with S. platensis showing normal structure (H&E, ×400).

manifested by increase of sperm motility and count. Theimprovement of sperm parameters may be due to antioxidantcomponents of S. platensis [53, 54].

In conclusion, the protective actions of S. platensis againstarsenic are believed to originate from its free radical scav-enging, antioxidant activities, maintenance of antioxidantenzymes, and a decrease in the production of inflammatorymediators that are implicated in the pathogenesis of arsenic-induced testicular injury. Therefore, S. platensis represents apotential agent to prevent testicular injury and dysfunctioninduced by arsenic exposure.

Conflict of Interests

There is no conflict of interests regarding the publication ofthis paper.

Acknowledgments

The authors would like to thank Dr. Ibrahim EL-HazzaScientific Group, for their guidance and helping during theexperiment period. The authors would also like to extendtheir sincere appreciation to the Deanship of ScientificResearch at King Saud University for funding this ResearchGroup no. RGP-1435-093.

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